Microbial-type terpene synthase genes occur widely in nonseed land plants, but not in seed plants

Abstract

The vast abundance of terpene natural products in nature is due to enzymes known as terpene synthases (TPSs) that convert acyclic prenyl diphosphate precursors into a multitude of cyclic and acyclic carbon skeletons. Yet the evolution of TPSs is not well understood at higher levels of classification. Microbial TPSs from bacteria and fungi are only distantly related to typical plant TPSs, whereas genes similar to microbial TPS genes have been recently identified in the lycophyte Selaginella moellendorffii. The goal of this study was to investigate the distribution, evolution, and biochemical functions of microbial terpene synthase-like (MTPSL) genes in other plants. By analyzing the transcriptomes of 1,103 plant species ranging from green algae to flowering plants, putative MTPSL genes were identified predominantly from nonseed plants, including liverworts, mosses, hornworts, lycophytes, and monilophytes. Directed searching for MTPSL genes in the sequenced genomes of a wide range of seed plants confirmed their general absence in this group. Among themselves, MTPSL proteins from nonseed plants form four major groups, with two of these more closely related to bacterial TPSs and the other two to fungal TPSs. Two of the four groups contain a canonical aspartate-rich "DDxxD" motif. The third group has a "DDxxxD" motif, and the fourth group has only the first two "DD" conserved in this motif. Upon heterologous expression, representative members from each of the four groups displayed diverse catalytic functions as monoterpene and sesquiterpene synthases, suggesting these are important for terpene formation in nonseed plants.terpene synthase | specialized metabolism | nonseed plant | gene evolution T erpenoids are the largest class of land plant secondary metabolites, but they are not uniformly distributed in the plant kingdom (1). Many seed plants (angiosperms and gymnosperms) produce terpenoids of diverse types in large quantities. However, among nonseed plants, only liverworts are known as copious producers of terpenoids (2). Terpenoids have diverse biological and ecological functions with many serving as chemical defenses against herbivores and pathogens (3, 4). Some have lineagespecific functions, such as the volatile terpenoids in flowers that are involved in attracting pollinators (5). Characterizing the biosynthesis of terpenoids in all plant lineages is therefore an important avenue to understanding their roles in the adaptation of various lineages of terrestrial plants.Terpene synthases (TPSs) are pivotal enzymes for terpenoid biosynthesis, forming a distinctive superfamily based on both sequence identity and structure classification. However, within this group, typical plant and microbial (bacterial and fungal) TPSs share very low sequence similarity and are therefore only distantly related (6). The typical plant TPSs form subfamilies with individual subfamilies generally associated with specific biochemical functions, such as monoterpene, sesquiterpene, or diterpene biosynthesis (7,8). Monoterpene synthases a...

Terpene Biosynthesis in Red Algae Is Catalyzed by Microbial Type But Not Typical Plant Terpene Synthases

“…www.plantphysiol.org/cgi/doi/10.1104/pp.18.01413 typical plant terpene synthase were first isolated in the early 1990s, and their sequences, expression, evolution, and encoded enzyme activities are well understood (Facchini and Chappell, 1992;Bohlmann et al, 1998;Trapp and Croteau, 2001;Chen et al, 2011). In contrast, MTPSL genes were discovered only recently (Li et al, 2012;Jia et al, 2016) and are more closely related to terpene synthase genes from bacteria and fungi than to typical plant terpene synthase genes (Li et al, 2012). The enzymes encoded by both typical plant terpene synthase and MTPSL genes convert the isoprenyl diphosphates, geranyl diphosphate (GPP; C 10 ), farnesyl diphosphate (FPP; C 15 ), and geranylgeranyl diphosphate (GGPP; C 20 ), to monoterpenes, sesquiterpenes, and diterpenes, respectively.…”

“…The enzymes encoded by both typical plant terpene synthase and MTPSL genes convert the isoprenyl diphosphates, geranyl diphosphate (GPP; C 10 ), farnesyl diphosphate (FPP; C 15 ), and geranylgeranyl diphosphate (GGPP; C 20 ), to monoterpenes, sesquiterpenes, and diterpenes, respectively. Typical plant terpene synthase genes are ubiquitous in land plants, whereas MTPSL genes appear to occur only in nonseed plants (Jia et al, 2016). A recent study by Kersten et al (2017) reported for the first time the identification of several terpene synthase genes from the transcriptomes of the red macroalgae Laurencia pacifica and Laurencia dendroidea in the class Florideophyceae.…”

“…edu/porphyridium) were downloaded to a local sever and searched using three conserved terpene synthase PFAM motif sequences: the N-terminal domain (PF01397), the metal-binding domain (PF03936), and trichodiene synthase (PF06330), by an HMM method as described previously (Jia et al, 2016). Transcriptomes of 27 red algae species were downloaded from the OneKP (https://sites.google.com/a/ualberta.ca/onekp/; Matasci et al, 2014) and processed as described previously (Jia et al, 2016). The longest open reading frame for each contig was identified and translated into a peptide, and then an HMMER search was used to find putative terpene synthases.…”

“…The same data set of terpene synthases from bacteria, fungi, Dictyostelium spp., Naegleria gruberi, and microbial-type TPSs from nonseed plants, excluding those from group V as described (Chen et al, 2016;Jia et al, 2016), was used for phylogenetic reconstruction together with PpMTPSL, EaMTPSL1/2, and six Laurencia spp. MTPSLs.…”

Oil body formation inMarchantia polymorphais controlled by MpC1HDZ and serves as a defense against arthropod herbivores

“…Within down-regulated genes associated with secondary metabolism (Figure 5A) and down-regulated in both experiments, we found five Mp TPS (Figure 5A), including mono- and di-TPS with a bacterial, fungal or plant origin [33, 59]. We also detected other genes involved in the biosynthesis of terpene precursors, including a deoxyxylulose 5-phosphate synthase ( Mp4g14720 , Mp DXS ) and a cis-prenyltransferase ( Mp3g18510 , Mp CPT5 ) gene (Figure 5A).…”